Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain

PLoS Biol. 2017 Apr 19;15(4):e2001573. doi: 10.1371/journal.pbio.2001573. eCollection 2017 Apr.

Abstract

All vertebrate brains develop following a common Bauplan defined by anteroposterior (AP) and dorsoventral (DV) subdivisions, characterized by largely conserved differential expression of gene markers. However, it is still unclear how this Bauplan originated during evolution. We studied the relative expression of 48 genes with key roles in vertebrate neural patterning in a representative amphioxus embryonic stage. Unlike nonchordates, amphioxus develops its central nervous system (CNS) from a neural plate that is homologous to that of vertebrates, allowing direct topological comparisons. The resulting genoarchitectonic model revealed that the amphioxus incipient neural tube is unexpectedly complex, consisting of several AP and DV molecular partitions. Strikingly, comparison with vertebrates indicates that the vertebrate thalamus, pretectum, and midbrain domains jointly correspond to a single amphioxus region, which we termed Di-Mesencephalic primordium (DiMes). This suggests that these domains have a common developmental and evolutionary origin, as supported by functional experiments manipulating secondary organizers in zebrafish and mice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Evolution
  • Body Patterning / genetics
  • Brain / embryology*
  • Brain / metabolism
  • Chick Embryo
  • Embryo, Nonmammalian / embryology*
  • Embryo, Nonmammalian / metabolism
  • Gene Expression Regulation, Developmental
  • In Situ Hybridization, Fluorescence
  • Lancelets / embryology*
  • Lancelets / metabolism
  • Male
  • Mice, Knockout
  • Models, Biological
  • Models, Genetic
  • Neural Tube / embryology*
  • Neural Tube / metabolism
  • Vertebrates / embryology*
  • Vertebrates / metabolism
  • Zebrafish

Grants and funding

Spanish Ministry of Economy and Competitiveness and European FEDER funds (grant number BFU2014-57516-P). To Luis Puelles and Jose Luis Ferran. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. European Research Council (grant number ERC-StG-LS2-637591). To Manuel Irimia. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Spanish Ministry of Economy and Competitiveness (grant number SEV-2012-0208).Centro de Excelencia Severo Ochoa (to CRG, Manuel Irimia). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Spanish Ministry of Economy and Competitiveness (grant number BFU2014-58908-P). To Jordi Garcia-Fernadez. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Seneca Foundation, Comunidad de Murcia (grant number 19904/GERM/15). To Luis Puelles. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Generalitat de Catalunya (grant number). ICREA Academia Prize to Jordi Garcia-Fernandez. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Spanish Ministry of Economy and Competitiveness (grant number BFU2013-43213-P). To Paola Bovolenta. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Spanish Ministry of Economy and Competitiveness (grant number BFU2014-55076-P). To Manuel Irimia. Including an FPI PhD fellowship to Laura Lopez-Blanch. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Marine Alliance for Science and Technology Scotland (MASTS) (grant number). To Ildiko Somorjai. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.